Use of disposable masks against Staphylococcus aureus in the chicken slaughter industryABSTRACT:
The present study evaluated the effectiveness of using disposable masks in mitigating the spread of Staphylococcus aureus during the chicken cutting process in a large poultry abattoir. The identification of carriers of S. aureus and the influence of the time of use of disposable masks was carried out. Contamination of utensils and equipment by S. aureus and products by mesophilic aerobes was determined, with and without the use of masks. The efficiency of different commercial masks was evaluated against S. aureus under simulated conditions. The results revealed that 36% of workers on processing lines at the abattoirs carried S. aureus. An increase in S. aureus counts was observed in masks worn by employees for up to 3 h. The transfer of microbial load to utensils was enhanced in the absence of the mask and over time. The breast fillets evaluated showed no difference in the count of mesophilic bacteria with and without the use of masks by employees, conversely, the cuts of thigh and drumstick, thigh fillet and drumstick and wings showed a significant difference with average counts lower than 2 .96 Log CFU/g. Tests under simulated conditions demonstrated the effectiveness of commercial masks in retaining microorganisms. The test mask used by the abattoirs proved to be inefficient, allowing the passage of sprays containing S. aureus, at 6, 15 and 25 cm, with 2.53, 1.74 and 0.66 Log CFU/plate, respectively. This mask saturated, creating a barrier effect that increased contamination in the employees’ work area.
Key words:
Staphylococcus aureus; chicken cuts; food safety; disposable masks
RESUMO:
O presente estudo avaliou a eficácia do uso de máscaras descartáveis na mitigação da propagação de Staphylococcus aureus durante o processo de corte de frango em um grande abatedouro de aves. Foi realizada a identificação de portadores de S. aureus e influência do tempo de uso de máscaras descartáveis. A contaminação em utensílios e equipamentos por S. aureus e produtos por aeróbios mesófilos foi determinada, com e sem uso de máscaras. A eficiência de diferentes máscaras comerciais foi avaliada contra S. aureus em condições simuladas. Os resultados revelaram que 36% dos trabalhadores das linhas de processamento no frigorífico eram portadores de S. aureus. Foi observado aumento na contagem de S. aureus em máscaras usadas pelos funcionários até 3 horas. A transferência de carga microbiana para utensílios foi potencializada na ausência da máscara e com o passar do tempo. Os filés de peito avaliados não apresentaram diferença na contagem de bactérias mesófilas com e sem o uso de máscaras pelos funcionários, por outro lado, os cortes de coxa e sobrecoxa, filé de coxa e sobrecoxa e asas apresentaram diferença significativa com contagens médias inferiores a 2,96 Log de UFC/g. Testes de condições simuladas demonstraram a eficácia das máscaras comerciais na retenção de microrganismos. A máscara teste utilizada pelo frigorífico mostrou-se ineficiente, permitindo a passagem de pulverizações contendo S. aureus, a 6, 15 e 25 cm, com 2,53, 1,74 e 0,66 Log UFC/placa, respectivamente. Essa máscara saturava, criando um efeito barreira que aumentava a contaminação na área de trabalho dos funcionários.
Palavras-chave:
Staphylococcus aureus; cortes de frango; segurança dos alimentos; máscaras descartáveis
INTRODUCTION
The quality of food serves as a competitive differentiator among companies in the market, given that consumers are becoming more discerning in meeting their expectations when acquiring products. The implementation of tools such as Good Manufacturing Practices (GMP), Standard Operating Procedures (SOP), and Hazard Analysis and Critical Control Points (HACCP) further strengthens the assurance of quality in the final product (OLIVEIRA et al., 2021). However, the handling of these products during processing may lead to an increase in the counts of deteriorating mesophilic aerobic bacteria and pose a risk of contamination by pathogens such as Staphylococcus aureus (PIEREZAN et al., 2022). The dissemination of S. aureus is closely associated with food handlers, as this agent is found on the skin, in the throat, nasal mucosa, and intestinal tract of healthy individuals (LAUX et al., 2019; BENCARDINO et al., 2021; MARTINS et al., 2024). Several studies have noted the presence of S. aureus in various types of meat sold in different commercial establishments (DEFLORIO et al., 2021). However, there is limited research on the presence of this microorganism in meats undergoing processing in industrial slaughtering units.
The utilization of personal protective equipment (PPE), especially disposable masks, to optimize GMP and reduce contamination by S. aureus, is a topic under discussion. Generally, procedures related to GMP are acknowledged by various authors as the primary factor responsible for maintaining product quality, including within the slaughtering industry (HOLAH, 2023). RAHMAN et al. (2022) mention the utilization of disposable masks in food processing for tasks requiring a higher level of hygiene to minimize the likelihood of respiratory contamination by operators during the processing of the product. The use of masks and gloves resulted in a 35% reduction in S. aureus nasal colonization levels, accompanied by a significant decrease in the incidence of hand contamination among food handlers (HO et al., 2015). According to KADARIYA et al. (2014), any operator handling end-products is obligated to use disposable masks to prevent or reduce the potential contamination by microbiological agents that can be transmitted from the handler to the food.
However, Resolution Nº 275 (BRAZIL, 2002), addressing the Technical Regulation of Good Manufacturing Practices, and Ordinance 368 (BRAZIL, 1997), the Technical Regulation on Hygienic-Sanitary Conditions and Good Practices for Manufacturing Establishments in Food Processing Industries, do not specify the mandatory use of disposable masks during food processing. According to PARRA (2013), the use of disposable masks may lead to increased contamination. After 15 to 30 min of use, humidification causes the fibers of the mask to stick together, creating virtual spaces that facilitate the passage of mucosa with microorganisms. Additionally, there is an accumulation of carbon dioxide, which can be irritating to mucous membranes, resulting in excessive coughing and itching in the nose, consequently leading to greater contamination. This also increases the contact of hands with the nostrils, further contributing to the contamination of the fingers by S. aureus.
Despite the ongoing discussion about the use of disposable masks, there is a literature gap concerning their efficacy in chicken slaughterhouses, and there is no official publication citing the mandatory use of these masks to ensure product quality. Therefore, this study evaluated the prevalence of S. aureus in the chicken cutting process, assessed the microbial count on masks, utensils, and processing mats, and compared the levels of aerobic mesophilic bacteria in products with and without the use of disposable masks within a large chicken slaughtering unit. Furthermore, the study assessed the effectiveness of various disposable masks under simulated conditions.
MATERIALS AND METHODS
To evaluate the efficacy of disposable masks in chicken processing, an analysis was conducted on disposable masks, utensils, and chicken cuts (Figure 1) in a large poultry abattoir unit in southern Brazil. Samples were collected from an industrial line during processing, both with and without the use of disposable masks.
Experimental design of the evaluation of the use of disposable masks in the count of S. aureus and mesophilic bacteria in the products and surfaces of a poultry slaughtering unit.
Identification of S. aureus carriers and the influence of the time of use of disposable masks
To identify S. aureus carriers and assess the influence of the duration of disposable mask usage, 100 single-use polypropylene masks with one elastic band were utilized in the chicken cutting lines. After 30 minutes of use, the masks were collected, individually packed in sterile bags, and subjected to S. aureus analysis. Individuals whose disposable masks exhibited S. aureus contamination were identified as carriers. To evaluate the escalation of contamination in the masks concerning the duration of use, disposable masks from the same 100 employees were collected after 60 and 180 minutes, following the same procedure. New masks were analyzed at time zero. Contamination was quantified in colony-forming units per mask (CFU/mask), considering only the masks with positive counts from carrier individuals.
Analysis of S. aureus on utensils and equipment
Contamination with S. aureus was assessed on the cutting boards, knives, and cutting mats used by employees on the processing lines for chicken breast and drumstick fillets, wings, and bone-in drumsticks. Swabs (3M, Quick swab model) with a 20 cm² delimiter were employed, and the results were expressed in CFU/cm². The high-density polyethylene cutting boards were cleaned every 120 minutes by soaking them in an alkaline detergent solution (1.5%) for at least 10 minutes, followed by scrubbing and rinsing with hot water at approximately 60 ºC before use. Stainless steel knives underwent a similar cleaning process every 120 minutes, involving soaking in an alkaline detergent solution (1.5%) for at least 10 minutes, followed by soaking in hot water at 85 ºC.
The polyurethane cutting mats were equipped with a chlorinated drinking water system (0.2 to 2 ppm) at room temperature, with a water flow rate of approximately 120 L/h. They underwent two cleaning processes each day: one with a direct blast of hot water (55 ºC) and another involving scrubbing with alkaline detergent (0.5%) and rinsing with hot water at 55 ºC. After slaughter, they were sanitized with a 2.0% peracetic acid solution. Evaluations of utensils and equipment were conducted with all employees wearing masks, followed by assessments without masks to compare the effectiveness of the results.
To evaluate the influence of utensil usage time on microbial contamination, swabs were collected from knives (from the stainless-steel blade) and cutting boards (from the central part of the board, where contact with the product occurs) at 0, 60, and 120 minutes of work. Twenty knives and 20 boards were sampled for each of the cutting lines (fillets of drumstick and breast, and bone-in drumsticks) at each time point. The maximum time considered was two hours, as all utensils in use were replaced after this period to minimize the potential for industrial contamination. No swab collection of utensils was conducted on the wing processing line, as it does not use knives and boards; wings are directly packed whole or cut by automatic equipment. To assess S. aureus contamination on the mats, swab collections were performed at 0, 60, and 120 minutes on the processing lines for drumstick and breast fillets, wings, and bone-in drumsticks. The collections were carried out directly at the point of the conveyor belt where the cut pieces were passing.
Analysis of aerobic mesophilic bacteria in chicken cuts
The cut samples were directly collected from the processing lines and placed in sterile collection bags, maintaining a controlled ambient temperature ranging from 10.5 ºC to 11.8 ºC. Triple samplings of breast and drumstick fillets, as well as wings and bone-in drumsticks of chicken, were conducted at times zero, 60, 120, 180, 240, and 300 min of processing. Product evaluations were initially performed with 100% of employers in the sector using masks, and subsequently, without using them, to facilitate a comparison of efficacy between the results. The products underwent a count of aerobic mesophilic bacteria to provide a more comprehensive set of results. All analyses were conducted in the company’s internal laboratory.
Efficiency of different commercial disposable masks against S. aureus
To evaluate the efficacy of disposable masks against S. aureus, an in vitro test was conducted in a simulated laboratory condition using four types of masks: Mask 1 (simple, 100% polypropylene, two elastic), Mask 2 (triple, 100% polypropylene, two elastic), Mask 3 (triple with filter, polypropylene, two elastic), and Mask 4 (model used by the abattoir, single, polypropylene, one elastic). For positive control, an experiment without a mask was conducted. For this study, an apparatus was developed comprising a stainless steel box (30 x 20 x 20 cm), as illustrated in figure 2, with a front opening (4 x 4 cm) where the masks were affixed, and the other end of the box left open.
Schematic of the apparatus used to perform the efficacy tests of disposable masks in simulated conditions.
To evaluate the effectiveness of different disposable masks in retaining S. aureus, the masks were securely positioned in the box, and a standard concentration of bacteria solution (approximately 3 Log CFU/mL) was sprayed through each test mask. Plates containing culture medium were then strategically placed at three different distances from the front opening of the mask: near (6 cm), medium (15 cm), and far (25 cm). After incubation, the plates were examined, and the bacterial counts were compared. The positions of the plates inside the box were carefully arranged to simulate the typical distance between an operator on the production line and the product. Each test was conducted in triplicate for every type of disposable mask assessed.
Microbiological analysis
The S. aureus counts were conducted following Official Method 2003.07 (AOAC, 2003) using the Staph Count Express plate (kit 3M™ Petrifilm™ STX Staph Express) as the culture medium. This test specifically detects coagulase-positive staphylococci, with enumeration involving the observation of red-violet colonies and/or pink halos on the plates after a 24-hour incubation period at 37 ºC. For counting aerobic mesophilic bacteria, analyses were performed using Plate Count Agar (Merck, Germany) as the culture medium, which was also incubated for 24 hours at 37 ºC (SILVA et al., 2017). The results were expressed in CFU/g and Log CFU/g.
Statistical analysis
The microbial count results at different times underwent ANOVA followed by Tukey’s test for statistical analysis. Additionally, comparisons for each treatment with and without disposable masks were conducted using Student’s t-test, both with a 95% confidence level.
RESULTS AND DISCUSSION
Identification of S. aureus-carrying employees
The percentage of individuals carrying S. aureus in the large poultry abattoir, specifically on the lines processing breast and drumstick fillets, wings, and bone-in drumsticks of chicken, was found to be 36%. This poses a risk of cross-contamination due to physical contact between individuals, such as personal greetings among colleagues, and job-sharing through rotating positions in the processing lines, which occurs every 30 min.
It is important to note that individuals can be asymptomatically colonized by S. aureus, falling into different classifications: persistent (10-20%), intermittent (30-50%), or non-carrier. Regardless of the classification, colonization poses a significant risk factor for food contamination (BENCARDINO et al., 2021). LAUX et al. (2019) reported that a third of the population carries S. aureus, based on a study conducted among health professionals. While several factors influencing S. aureus carrier status has been identified, but the reason why only some people are colonized remains unclear. Based on these results, new experiments were conducted to assess the effectiveness of using masks in controlling contamination by S. aureus. The identification of a significant percentage of S. aureus carriers highlights the critical need for rigorous hygiene measures and continued surveillance in poultry processing facilities to prevent microbial contamination and ensure the production of safe and healthy poultry products for consumers.
The count of S. aureus in disposable masks over time
Figure 3 illustrates the S. aureus counts in employees’ disposable masks at 0,60, and 180 minutes of use by carriers. An increase in S. aureus colony-forming units (CFUs) in the masks over time is evident, indicating a linear positive correlation between the duration of use and the CFU count (Pearson’s correlation coefficient = 0.94). However, a high standard deviation is observed due to the variation in microbial load among users. This escalating count in disposable masks could contribute to the cross-contamination of utensils (cutting boards, knives, and processing mats) as well as the products. The level of contamination varies based on the behavior of the product handlers, particularly through hand contact with the mask, which tends to become saturated with S. aureus in carriers. Due to the scarcity of studies evaluating the use of masks in chicken slaughter units, the results of this research were compared with a study that investigated the use of masks in surgical procedures regarding the count of S. aureus. In that study, it was observed that surgical masks exhibited bacterial growth over time, with the highest percentage (80%) observed after 2 and 4 hours (PUTRI et al., 2023).
S. aureus counts in disposable masks at different times of use in industrial lines of chicken cuts.
S. aureus counting on the utensils and equipments in chicken cutting lines
Counting was conducted on the cutting boards for breast fillet, drumstick fillet, and bone-in drumsticks, both with and without mask usage at different times (Figure 4A). The count at 60 min was exclusively performed for breast fillets due to the higher number of employees in that processing line. The count at 120 min was done for all cuts without the use of disposable masks, indicating that this duration is sufficient for the microorganism to reach the cutting board in the employees’ handling area. The counts for the cutting of bone-in drumsticks at 120 min with masks can be attributed to the saturation of the mask’s retention capacity against the microorganism. It is plausible to suggest that disposable masks may have a saturation limit for retaining microorganisms, and beyond that, the excess load may pass through the mask material or be expelled from the side of the mask along with the users’ respiratory flow.
Counting of S. aureus in cutting boards (A), knives (B), and cutting mats (C) of cuts of chicken with masks (WM) and without masks (WTM) at different production times.
S. aureus counts on knives (Figure 4B) without the use of masks over time were observed for the cutting of breast and drumstick fillets. Meanwhile, counts of S. aureus with the use of disposable masks was observed only for the cutting of drumstick fillets. At 120 min without masks, a higher count of knives was noted compared to 60 min, facilitated by the direct and constant contact of the utensil with the hands of the employees. For the cutting of drumstick fillets, counting after 120 min with the use of disposable masks was observed, possibly justified by the saturation of the mask, leading to the passage of microorganisms to the utensil. Another possibility is cross-contamination of the utensil by the cutting piece due to the flow of the processing line, where each cut is handled by up to 5 employees before packaging.
S. aureus counts were observed on the processing mats without the use of masks over time for the cutting of wings and bone-in drumsticks (Figure 4C). The drumstick fillet mat showed counts with the use of masks from the 120 min mark. In general, the irregularity of the results does not allow for a specific treatment of absences and/or counting at different times, with or without masks. These variations may be attributed to self-flushing with water on each of the mats with a variable removal capacity of the microorganisms.
The results depicted in Figure 3 underscores the significance of mask usage, thereby suggesting their replacement every 120 min, alongside the implementation of rigorous hand hygiene protocols and regular disinfection of equipment and surfaces. These measures are crucial for mitigating the spread of pathogens and safeguarding both the health of employees and the quality of poultry products. In this context, considering that S. aureus bacteria can be carried by healthy individuals, the utilization of respiratory masks emerges as a viable option to diminish the risk of contamination in food production areas, as recommended by the European Food Safety Authority (EFSA, 2009).
Assessment of aerobic mesophilic bacteria in products
In the samples of breast fillet (Table 1) produced by employees using disposable masks, a notable increase in the count of aerobic mesophilic bacteria was observed at the 300-minute mark compared to shorter durations. Without masks, the bacterial count increases after a shorter period, becoming significant from 240 minutes onwards. However, there was no significant difference (P > 0.05) between the treatments with and without masks at different time intervals, nor in the mean bacterial counts between the two treatments. For drumstick fillets, a similar trend was observed with the disposable mask treatment, showing significant (P < 0.05) growth in bacterial counts at 300 minutes. Notably, a significant increase in microorganism count was already evident at 120 minutes when disposable masks were not utilized. Additionally, a significant difference (P < 0.05) was observed between the mean bacterial counts in the treatments with and without disposable masks. In the case of bone-in drumsticks, significantly higher bacterial counts were observed after 180 minutes without the use of disposable masks, whereas no notable increase in count was observed in the treatment where masks were used.
The wing cuts exhibited a disparity in the distribution of the results, with no significant difference (P > 0.05) observed for the counts without the use of disposable masks, even over time. However, a notable increase was observed at 300 min with masks. These findings may be attributed to the limited handling of this chicken cut (involving only 2 employees) and the shorter processing time before packaging. Interestingly, significantly greater contamination was observed in the treatment without masks compared to the treatment with masks for this particular chicken cut.
In general, it was found that bacterial counts were higher without the use of masks for all cut items except breast fillet. A statistically significant difference (P < 0.05) was noted for cuts of drumstick fillets and wings between treatments with and without disposable masks. The utilization of disposable masks, along with clean uniforms, gloves, and proper operator hygiene, is considered essential for preserving the microbiological quality of meat (FAO, 2017). The results highlighted a significant reduction in microbial counts (Table 1) when employees used masks for 300 minutes, contributing to compliance with sanitary requirements and market standards. Therefore, the implementation of disposable masks remains crucial to ensuring food safety. Both sets of results, with and without disposable masks, met the sanitary requirements outlined in Anvisa’s Normative Instruction Nº 161, dated July 1, 2022 (BRAZIL, 2022). This regulation establishes a standard mesophilic aerobic bacteria count of 1 x 105 CFU/g (5 Log CFU/g) for poultry meat.
Effectiveness of various commercial disposable masks against S. aureus in simulated conditions
For the tests conducted under simulated conditions (Table 2), a significant negative correlation of -0.99 was observed between not using a mask and using disposable mask 4, which is the model utilized by the company. This correlation indicates a strong relationship between the absence of a mask and increased bacterial counts compared to using the specified disposable mask. In these simulated tests (Table 2), masks 1, 2, and 3 showed no growth of S. aureus, regardless of the distance between the masks and the count plates. This result suggests their effectiveness in retaining the aqueous solution of S. aureus. Conversely, in the absence of a disposable mask, S. aureus counts at both mean and far distances were significantly higher compared to counts at close distances, highlighting the lack of a barrier against the spray in the no-mask condition.
With disposable mask 4, the volume of microorganisms decreases as the spray application distance increases. The far count value in the test without masks is nearly 100 times greater than that for mask 4, reflecting the barrier effect generated by the mask under test, which leads to partial retention of the spray but allows the passage of some droplets. Simultaneously, the near count is 3.55 times greater with mask 4 than without it, confirming the barrier effect. This allows the passage of microorganisms, resulting in the contamination of the employee’s handling area (cutting boards, knives, and mats), and, consequently, the processed product.
The use of mask 4 may exacerbate contamination by the microorganism in areas close to employees. This result highlighted the disposable mask’s inability to completely retain microorganisms, potentially compromising the product’s quality. This finding is consistent with PARRA (2013), who discusses an increase in the count with mask usage due to humidification and saturation, allowing saliva droplets to pass into the handling environment. In conclusion, the effectiveness of disposable masks in chicken cut processing lines depends on the quality and time of replacement of these masks.
Based on the results obtained, masks 1 (simple, 100% polypropylene, two elastic), 2 (triple, 100% polypropylene, two elastic), and 3 (triple with filter, polypropylene, two elastic) demonstrate effectiveness in preventing the passage of microorganisms, irrespective of the spraying distance. Therefore, these masks can be recommended for use in food production units.
CONCLUSION
The study found that 36% of individuals working in chicken cut lines were carriers of S. aureus. The count of S. aureus in evaluated masks increased over time from 51 CFU/disposable masks at 60 min to 81 CFU/disposable masks at 180 min. Evaluation results for cutting boards, knives, and mats showed contamination by S. aureus when employees did not use disposable masks, except for bone drumsticks in cutting boards, drumstick fillet knives, and drumstick fillet processing mats. These contaminations may be due to failures in GMP, which recommends changing masks every 120 min. Contamination in the products by aerobic mesophilic bacteria was observed in all cuts; however, the levels were lower in samples processed by employees with masks. In a simulated condition of the commercial mask models tested against S. aureus showing total retention efficiency against spray.
This study emphasized the significance of following GMP guidelines, especially regarding the use of masks, to reduce the risk of contamination in poultry processing facilities. Moreover, the effectiveness of masks in decreasing bacterial contamination showed their function in maintaining food safety and hygiene standards.
ACKNOWLEDGMENTS
This study was financed in part by the Conselho Nacional de Desenvolvimento Científico e Tecnológico - Brasil (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Financing Code 001 and Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul - Brasil (FAPERGS)
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Edited by
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Editors: Rudi Weiblen (0000-0002-1737-9817) Juliana Felipetto Cargnelutti (0000-0002-3160-3643)
Data availability
The data that support the findings of this study are available from: https://docs.google.com/document/d/1rxrz3DjyjbbsYvOQH9F_8AT0yFbQtOCl/edit?usp=sharing&ouid=118274776851360093361&rtpof=true&sd=true.
Publication Dates
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Publication in this collection
11 Nov 2024 -
Date of issue
2025
History
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Received
18 Dec 2023 -
Accepted
21 July 2024 -
Reviewed
23 Sept 2024
